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Home , Eciton burchellii, Ectatomminae, Manica (genus), Manica rubida, Myrmeciinae, Myrmica lobicornis

Russian Entomol. J. 26(1): 49–62 © RUSSIAN ENTOMOLOGICAL JOURNAL, 2017

The metathoracic spiracles in some and (: Formicidae; Vespidae)

Ìåòàòîðàêàëüíûå äûõàëüöà íåêîòîðûõ ìóðàâüåâ è îñ (Hymenoptera: Formicidae; Vespidae)

Elena B. Fedoseeva Åëåíà Á. Ôåäîñååâà

Zoological Museum of Lomonosov Moscow State University, Bolshaya Nikitskaya Street 2, 125009 Moscow, Russia. Зоологический музей МГУ им М.В. Ломоносова, Большая Никитская ул., 2, 125009 Москва, Россия.

KEYWORDS: , Comparative anatomy, mesosoma, mesopleuron, metapleuron, spiracular mechanism. КЛЮЧЕВЫЕ СЛОВА: Aculeata, сравнительная морфология, мезосома, мезоплеврон, метаплеврон, механизм дыхальца.

ABSTRACT. The second thoracic spiracle and the мы со скрытыми дыхальцами из обоих семейств adjacent skeleton were studied in twenty-two Aculeata имеют запирающую дыхальцевую мышцу в from nine Formicidae subfamilies (, Doli- дополнение к супрамезоплевральному склериту, choderinae, , Paraponerinae, , Ec- скрывающему истинное дыхальце. Предполагается tatomminae, , and Ecitoninae) and гомология между повторно обнаруженной дыхаль- two species from Vespidae (Vespa crabro L., 1758 цевой мышцей Aculeata и соответствующей мышцей and sp.). Dissections followed by scan- метаторакального дыхальца Symphyta. Сравнение ning electron microscopy or photography revealed that крылатых Formicidae и рабочих муравьев со скрыты- the studied alate forms with concealed spiracles from ми дыхальцами продемонстрировало сходство меж- both Aculeata families possess the spiracular occlusor ду ними как по положению пластинок, покрываю- muscle in addition to the supramesopleural sclerite con- щих дыхальца (т.е. супрамезоплеврального склерита cealing the true spiracle. There is assumed to be a homol- и дыхальцевой лопасти, соответственно), так и по ogous relationship between the re-discovered spiracular положению дыхальцевых мышц. Поэтому дыхальце- occlusor muscle of Aculeata and the corresponding mus- вую лопасть рабочих муравьёв Formicinae, Dolicho- cle of the metathoracic spiracle in Symphyta. The com- derinae, Myrmeciinae, Paraponerinae, Ponerinae, Ecta- parison of winged Formicidae and ant workers with tomminae следует считать дериватом супрамезоплев- concealed spiracles demonstrated the similarities be- рального склерита, присущего крылатым самкам. В tween them both on the position of plates covering the свою очередь, открытый тип дыхалец у рабочих му- metathoracic spiracles (i.e. supramesopleural sclerite and равьёв Myrmicinae, Dorylinae и Ecitoninae согласует- spiracular lobe, respectively), and on the position of the ся с отсутствием супрамезоплеврального склерита у spiracular occlusor muscles. Accordingly, the spiracular крылатых форм из тех же подсемейств. lobe of worker ants of Formicinae, , Myr- meciinae, Paraponerinae, Ponerinae and Introduction was determined to be a derivative of the supramesopleu- ral sclerite that is essential to their winged females. At the same time the exposed type of spiracles observed in As the metathoracic spiracles are inconspicuous or studied Myrmicinae, Dorylinae and Ecitoninae ant work- concealed, it is difficult to investigate their morphology ers corresponds with the absence of the supramesopleural and phylogeny in aculeate hymenoptera. Nevertheless, sclerite in the alate forms. their position is one of the important landmarks on the hymenoptera thorax [Reid, 1941]. In winged forms, the РЕЗЮМЕ. Второе грудное дыхальце и примыка- second thoracic spiracles are concealed beneath the bases ющий к нему скелет были изучены у 22 видов мура- of the hind wings; in wingless forms, the original position вьёв из 9 подсемейств Formicidae (Formicinae, of the spiracle is in the membrane between the meso- and Dolichoderinae, Myrmeciinae, Paraponerinae, Ponerinae, metapleuron. According to Reid, in many forms the Ectatomminae, Myrmicinae, Dorylinae и Ecitoninae), а second spiracle is at the dorsal termination of the me- также у двух видов ос из Vespidae (Vespa crabro L. sometapleural suture, and with very few exceptions it is 1758 and Dolichovespula sp.). Препаровка с последу- always at the junction of the dorsum and pleura. ющей сканирующей электронной микроскопией либо Meanwhile et Duncan [1939] noted that second thorac- фотосъёмкой показали, что изученные крылатые фор- ic spiracle of vespine wasps is covered by a small sclerite. 50 E.B. Fedoseeva

He referred to it as the spiracular peritreme, but subsequent spiracle, were analysed in the course of compiling the comparison with other Hymenoptera suggested that it is a attributes of species, genera and subfamilies [Yoshimura, real sclerite [Tonapi, 1958]. Primarily it was attributed to Fisher, 2007, 2012; Boudinot, 2015]. Information about the posterodorsal corner of the mesopleuron [Duncan, the status of this trait in females is published infrequently 1939; Tonapi, 1958]. However, currently, based on data of [Ogata 1987, 1991]. However the internal structure of the symphytans, modern authors referred to sclerite as certain metathoracic spiracle in Formicidae species is not men- intersegmentalia that were affiliated with the mesopleuron tioned in modern publications. [Vilhelmsen, 2000; Vilhelmsen et al., 2010]. Besides vespine wasps, the sclerite that conceals or partly covers Materials and methods the second thoracic spiracle was detected in some other taxa of Aculeata. As a result, it acquired a variety of denominations: collar [Tonapi, 1958]; epimeral lobe [Ri- The examined material included two wasp species chards, 1977; Yoshimura, Fisher, 2007]; basalar lobe from Vespidae (), Vespa crabro Linnaeus, [Bohart, Menke, 1976; Deyrup, Cover, 2004; MacGown 1758 and Dolichovespula sp., and twenty-three ant et al., 2014], supramesopleural sclerite [Vilhelmsen et species from nine subfamilies of Formicidae: Formici- al., 2010], spiracular sclerite [Boudinot, 2015]. nae, Dolichoderinae, Myrmeciinae, Paraponerinae, Pon- The mechanism of the second thoracic spiracle in erinae, Ectatomminae, Myrmicinae, Dorylinae and Aculeata representatives remains uncertain although many Ecitoninae (Table). Detailed information about speci- researchers have studied it. Most agree with certain sim- mens is presented in Appendix 1. ilarities between the second spiracle and the first one, in Table. List of examined Formicidae species which the aperture is regulated by a single occlusor Таблица. Список изученных видов Formicidae muscle. The principal disagreement concerns the exist- ence of the corresponding muscle. For example, there is Subfamily Species an occlusor muscle of the second thoracic spiracle in Dolichoderinae Azteca sp. several ant species [Nasonov, 1889; Tonapi, 1958, 1959; Dolichoderus attelaboides (Fabricius, 1775) Delye, 1965]. Duncan [1939], Tonapi [1958] and Rich- Dorylinae orientalis Westwood, 1835 ards [1977] noted the presence of the occlusor muscle in Ecitoninae burchellii (Westwood, 1842) vespine wasps while Snodgrass [1925] declared its ab- Ectatomminae tuberculatum (Olivier, 1792) sence in honeybees. In addition to above mentioned Formicinae Ñamponotus (Tanaemyrmex) sp. aculeates Tonapi [1958] studied spiracular structures in Ñamponotus herculeanus (Linnaeus, 1758) Symphyta species. Most of his conclusions relating to the Formica aquilonia Yarrow, 1955 Formica exsecta Nylander, 1846 presence of an occlusor muscle of the second thoracic Formica lugubris Zetterstedt, 1838 spiracle in symphytans were corroborated [Vilhelmsen, Lasius niger (Linnaeus, 1758) 2000], but the muscle’s existence in aculeates requires Myrmeciinae sp. additional studies. The main problem is that it is such a Myrmecia piriformis Smith, F., 1858 minute muscle and is therefore difficult to detect. More- Myrmicinae Aphaenogaster gibbosa (Latreille, 1798) over, sometimes it “is not possible to discern between Atta sexdens (Linnaeus, 1758) concealment and absence of the spiracle because this rubida (Latreille, 1802) fragile structure was often destroyed during dissection” Messor denticulatus Santschi, 1927 [Vilhelmsen et al., 2010: 72]. lobicornis Nylander, 1846 Since the attributes of the metathoracic spiracle as Myrmica ruginodis Nylander, 1846 badius (Latreille, 1802) well as the state of its associated sclerite are important for Paraponerinae clavata (Fabricius, 1775) interpretation of Aculeata phylogeny, it was further eval- Ponerinae Diacamma geometricum Smith F., 1857 uated in this study. It was necessary to demonstrate the Ponerinae Dinoponera gigantean (Perty, 1833) adjacent skeleton and the components of the spiracle at least in representatives of the two families Vespidae and Formicidae. The number of species in Formicidae was Most of the material for the present study was pre- greater for the following reasons. Most Formicidae spe- served in 70% ethanol. Dried material was used in some cies have winged sex individuals (males and females) and instances. The dissections were carried out with tools for wingless workers (non-reproductive females), that mark- ophthalmic microsurgery (spring scissors, blade holder edly differed in thorax morphology. Moreover the thorax and forceps), pieces of razor blades and hair, and entomo- structure varies between Formicidae subfamilies. There- logical pins. Prior to dissecting the mesosoma, the head, fore it was necessary to study the representatives of legs, wings and metasoma were removed. Dissection of winged and wingless forms of different taxa. Meanwhile wet mounts was executed in Petri dishes (35×10 mm) recent work devoted to analysis of Formicidae morphol- filled with water under a stereomicroscope Olympus ogy and phylogeny included data only about the external SZ61. Dissected specimens were placed in 70% ethanol. state of the metathoracic spiracles — concealed or ex- Photographs of wet specimens were taken using a Leica posed — in ant workers [Keller, 2011]. The similar M165C stereomicroscope with a Leica DFC425 digital characteristics of Formicidae males, such as the presence camera, Z-stacked using Helicon Focus 4.10 at PIN RAS. or absence of sclerite concealing the second thoracic The preparations for scanning electron microscopy (SEM) Metathoracic spiracles in ants and wasps 51 were transferred from 70 to 99.9% ethanol in an ethanol mounted on SEM stubs, sputter-coated with gold and series and critical-point dried. The preparations were photographed using Tescan Vega TS5130MM scanning

1

2

3 4

Figs 1–4. Mesosoma and its spiracles in Vespidae, internal lateral view, anterior to the left: 1, 3 — Dolichovespula sp., worker; 2, 4 — Vespa crabro, worker. Abbreviations in Appendix 2. Рис. 1–4. Мезозосома и её дыхальца у Vespidae, латеральный вид изнутри, передний конец слева: 1, 3 — Dolichovespula sp., рабочая особь; 2, 4 — Vespa crabro, рабочая особь. Обозначения в Приложении 2. 52 E.B. Fedoseeva electron microscope at IPEE RAS. All images were In general, terminology follows The Hymenoptera edited in Adobe Photoshop CS2. Glossary represented at the site of the Hymenoptera

5 6

7 8

9 10 11

Figs 5–11. Mesosoma and its spiracles in alate Formicidae, lateral view, anterior to the left: 5–6 — Formica aquilonia (Formicinae), female; 7–8 — Camponotus sp. (Formicinae), female; 9–11 — Diacamma geometricum (Ponerinae), male. Abbreviations in Appendix 2. Рис. 5–11. Мезозосома и её дыхальца у крылатых Formicidae, латеральный вид изнутри, передний конец слева: 5–6 — Formica aquilonia (Formicinae), самка; 7–8 — Camponotus sp. (Formicinae), самка; 9–11 — Diacamma geometricum (Ponerinae), самец. Обозначения в Приложении 2. Metathoracic spiracles in ants and wasps 53

Anatomy Ontology project [Yoder et al., 2010]. As between the mesopleuron and the metapleuron; some terms have several interpretations, the chosen metapleural carina — the carina that delimits the definitions are below: metapleuron dorsally from the propodeum, extends mesopleuron — the area that is located lateral to the from just ventral to the metapleural arm to the meta- mesodiscrimen; coxal articulation and passes anteroventral to the metapleuron — the area of the metapectal-propodeal propodeal spiracle. complex that is located lateral to the metadiscrimen; Such terms like operculum, arm, and rim follow mesometapleural suture — the suture that is located Snodgrass [1925], who used them to differentiate com-

12

13 14

Figs 12–14. Mesosoma and its spiracles in alate ants and wasps: 12–13 — Paraponera clavata (Formicidae, Paraponerinae), female internal lateral view, anterior to the left; 14 — Dolichovespula sp. (Vespidae: Vespinae), worker, dorsal view, anterior to the left: the left metathoracic spiracle with inside-out supramesopleural sclerite. Abbreviations in Appendix 2. Рис. 12–14. Мезозосома и её дыхальца у крылатых муравьёв и ос: 12–13 — Paraponera clavata (Formicidae: Paraponerinae), самка, латеральный вид изнутри, передний конец слева; 14 — Dolichovespula sp. (Vespidae:Vespinae), рабочая особь, сверху, передний конец слева, левое метаторакальное дыхальце с вывернутым наружу супрамезоплевральным склеритом. Обозначения в Приложении 2. 54 E.B. Fedoseeva ponents of the first thoracic spiracle. Spiracular valves second spiracle. Other terms which are absent in the are undifferentiated closing plates of the entrance to the Glossary are given with references to the publications.

15 16

17 18

19

20

Figs 15–20. Mesosoma and its spiracles in alate Formicidae, lateral view, anterior to the left: 15 — left metathoracic spiracle of Dorylus orientalis (Dorylinae), male; 16 — the same, partly removed projections of meso- and metapleuron; 17–18 — (Myrmicinae), male; 19–20 — Myrmica ruginodis, female (Myrmicinae). Abbreviations in Appendix 2. Рис. 15–20. Мезозосома и её дыхальца у крылатых Formicidae, сбоку, передний конец слева: 15 — левое метаторакальное дыхальце Dorylus orientalis (Dorylinae), самец; 16 — то же, частично удалены лопасти мезо- и метаплеврона; 17–18 — Manica rubida (Myrmicinae), самец; 19–20 — Myrmica ruginodis, самка (Myrmicinae). Обозначения в Приложении 2. Metathoracic spiracles in ants and wasps 55

21 22

23

24

25

Figs 21–25. Mesosoma and its spiracles in Formicidae workers, lateral-dorsal view, anterior to the left: 21 — Formica exsecta (Formicinae); 22 — Dolichoderus attelaboides (Dolichoderinae); 23 — (Ectatomminae); 24 — Pogonomyrmex badius (Myrmicinae); 25 — Eciton burchellii (Ecitoninae). Abbreviations in Appendix 2. Рис. 21–25. Мезозосома и её дыхальца у рабочих Formicidae, сверху-сбоку, передний конец слева: 21 — Formica exsecta (Formicinae); 22 — Dolichoderus attelaboides (Dolichoderinae); 23 — Ectatomma tuberculatum (Ectatomminae); 24 — Pogonomyrmex badius (Myrmicinae); 25 — Eciton burchellii (Ecitoninae). Обозначения в Приложении 2. 56 E.B. Fedoseeva

Results Dolichoderinae, Paraponerinae and Ponerinae. Its shape varies from triangular to oval (Figs 5–11). In females Metathoracic spiracles of winged forms of Formica aquilonia, Camponotus herculeanus and Figs 1–20. Camponotus sp., a triangular plate firmly fixed be- tween the meso- and metapleuron has an orifice just The supramesopleural sclerite is clearly expressed opposite the spiracle opening (Figs 6–7) that is evident in both studied wasp species. A spiracle atrium fur- under high magnification (Fig. 8). As in vespine wasps, nished with a blocking hemispheric plate (operculum) is the spiracular mechanism of male Diacamma geomet- located in the membranous area beneath the sclerite. ricum (Figs 9–11) and female Paraponera clavata Although the diameter of the appropriate trachea is less (Figs 12–13) includes an operculum, a lower rim and a than in the mesothoracic spiracle (Figs 1–2), the aper- fan-shaped occlusor muscle, whose origin site is on the ture of the spiracular atrium is also regulated by the mesopleuron near the border with the supramesopleu- occlusor muscle. The origin of that small, fan-shaped ral sclerite. muscle, consisting of a few fibres, lies on the upper The male of Dorylus orientalis has no distinct su- posterior edge of the mesopleuron while the operculum pramesopleural sclerite, but the second thoracic spiracle is the site of its attachment (Figs 3–4; 14). possessing the operculum is protected by two opposite A differentiated supramesopleural sclerite was ob- outgrowths: an upper “lobe” related to the mesopleuron served in studied males and females of Formicinae, and a lower one related to the metapleuron (Figs 15–16). 26 27

28 29

Figs 26–29. Metathoracic spiracles in Formicidae workers, lateral-dorsal view, anterior to the left: 26 — Formica exsecta (Formicinae); 27 — Dolichoderus attelaboides (Dolichoderinae); 28 — Azteca sp. (Dolichoderinae); 29 — Ectatomma tuberculatum (Ectatomminae). Abbreviations in Appendix 2. Рис. 26–29. Метаторакальные дыхальца у рабочих Formicidae, сверху-сбоку, передний конец слева: 26 — Formica exsecta (Formicinae); 27 — Dolichoderus attelaboides (Dolichoderinae); 28 — Azteca sp. (Dolichoderinae); 29 — Ectatomma tuberculatum (Ectatomminae). Обозначения в Приложении 2. Metathoracic spiracles in ants and wasps 57

30 31 32

33 34

35 36

Figs 30–36. Metathoracic spiracles in Formicidae workers: 30–32 — left spiracle of Azteca sp. (Dolichoderinae); 30 — lateral-dorsal view, anterior to the left; 31 — skeletal details of the spiracular mechanism; 32 — ventral view of operculum; 33–34 — the left spiracle under two different magnifications, Eciton burchelli (Ecitoninae), lateral-dorsal view; 35–36 the right spiracle under low and high magnification, Aphaenogaster gibbosa (Myrmicinae), dorsal view, anterior to the left. Abbreviations in Appendix 2. Рис. 30–36. Метаторакальные дыхальца у рабочих Formicidae: 30–32 — левое дыхальце Azteca sp. (Dolichoderinae); 30 — сверху- сбоку, передний конец слева; 31 — скелетные части механизма дыхальца; 32 — снизу, вид на оперкулум; 33–34 — левое дыхальце Eciton burchelli (Ecitoninae) при двух разных увеличениях, сверху-сбоку; 35–36 — правое дыхальце при малом и большом увеличении, Aphaenogaster gibbosa (Myrmicinae), сверху, передний конец слева. Обозначения в Приложении 2. 58 E.B. Fedoseeva

The supramesopleural sclerite is also absent in males this spiracle with two hemispheric valves resembles the and females of examined Myrmicinae (Figs 17–20). second thoracic spiracle of some symphytans. The second thoracic spiracle lies in a membranous area Metathoracic spiracles of ant workers between the upper opposite edges of the meso- and Figs 21–49. metapleuron and is hardly visible because usually the pleural edges are are contiguous (Figs 18, 20). As it was Crucial changes in the structure of the mesosoma in possible to discern from a single dry specimen of a male ant workers due to the absence of flight muscles did not Atta sexdens (with pleural edges slid apart), externally affect the primary position of the second thoracic spira-

37 38

39 40

Figs 37–40. Metathoracic spiracles in Formicidae workers, internal lateral view, anterior to the left: 37–38 — Formica aquilonia (Formicinae); 39–40 — (Myrmeciinae). Abbreviations in Appendix 2. Рис. 37–40. Метаторакальные дыхальца у рабочих Formicidae, изнутри-сбоку, передний конец слева: 37–38 — Formica aquilonia (Formicinae); 39–40 — Myrmecia pyriformis (Myrmeciinae). Обозначения в Приложении 2. Metathoracic spiracles in ants and wasps 59

41 42

43 44

45 46

47 48 49

Figs 41–49. Metathoracic spiracles in ant workers of Myrmicinae: 41–42 — Myrmica lobicornis; 43–44 — Manica rubida; 45–46 — Atta sexdens; 47–48 — Messor denticulatus; 49 — Pogonomyrmex badius; 41– 46 — lateral view, anterior to the left; 47–48 — dorsal view; 49 — lateral-dorsal view. Abbreviations in Appendix 2. Рис. 41–49. Метаторакальные дыхальца у рабочих муравьёв Myrmicinae: 41–42 — Myrmica lobicornis; 43–44 — Manica rubida; 45–46 — Atta sexdens; 47–48 — Messor denticulatus; 49 — Pogonomyrmex badius; 41– 46 — сбоку, передний конец слева; 47–48 — сверху; 49 — сбоку-сверху. Обозначения в Приложении 2. 60 E.B. Fedoseeva cles. As in alate forms each one is located at an upper comparison of the external mesosomal structure between point of the mesometapleural junction (above the me- three types of ant females — alate, ergatoid queens and sometapleural pit) despite the fact that an appropriate workers in Myrmecia F., 1804 and Paltothyreus Mayr, suture between the meso- and metapleuron is often 1862 ants, executed by Emery [1900], pointed directly to scarcely detected or is absent (Figs 21–25). such a possibility. All examined second thoracic spiracles of workers of Nasonov [1889] was the first who noted the pres- Formicinae, Dolichoderinae, Ectatomminae, Ponerinae, ence of muscle in the second thoracic spiracle of the Paraponerinae and Myrmeciinae were positioned under Lasius flavus ant worker. Subsequently Tonapi [1958] differentiated plates [spiracular lobes — by Keller, 2011]. detected this muscle in spiracles of L. fuliginosus, The shape of the plate, forming a protective chamber over L.niger, Formica fusca ants and also in males of Dory- the true spiracle, may be markedly different, but the pres- lus labiatus [Tonapi, 1959]. But his images of the ence of either an orifice or gap is constant (Figs 26–29). spiracular mechanism were extremely schematic espe- The spiracular atrium opens into the chamber and has a cially in comparison with a more recent description blocking operculum (Figs 28, 30–32) with an attached executed by Delye [1965] on the Camponotus compres- occlusor muscle that regulates the atrium aperture. A small sus worker. Delye noted that the muscle originates on fan-shaped muscle consists of several fibres that originate the border of the plate covering the second spiracle and on the border of plate and the mesothorax (Figs 37–40). As also noted that the plate forms a chamber with a small in alate forms, the composition of skeletal structures form- orifice above the true spiracle. ing the true spiracle includes the operculum with the arm The present study demonstrated that the occlusor mus- (site of muscle insertion) and the rim (Figs 31–32). The cle attached to the operculum is really present in the operculum and immovable rim jointly encircle the atrium metathoracic spiracle at least in studied species of Vespinae entrance while muscle contraction regulates the split be- wasps and also in the representatives of Formicinae, Doli- tween them by moving the operculum in the same way as in choderinae, Myrmeciinae, Ponerinae, Paraponerinae and the mesothoracic spiracle. The origin site of the spiracular Ectatomminae ants. The muscle originates at the border of muscle as well as the close association between the plate the mesopleuron and supramesopleural sclerite (in females and metathoracic spiracle indicates that the spiracular lobe and males) or at the border of the mesopleuron and spirac- of workers is derived from the supramesopleural sclerite of ular lobe (ant workers). As both plates (i.e. supramesopleu- alate females. ral sclerite and spiracular lobe) occupy a similar position at In contrast to the above mentioned subfamilies the the mesosoma of winged forms and ant workers, respec- Myrmicinae workers have so-called exposed metatho- tively, and the muscles of the second spiracles in winged racic spiracles. Such a spiracle is hardly detected even in and wingless ants have a similar site of origin, the homol- major workers of Pogonomyrmex Mayr, 1868 and Mes- ogy between the supramesopleural sclerite and spiracular sor Forel, 1890. The spiracular atrium is located at a lobe becomes obvious. minute cuticular orifice surrounded by rugae, but in most According to modern research, the winged Myrmici- cases it becomes distinctly visible under high magnifica- nae castes (both males and females) have no distinct tion. It is equipped with two valves that are weakly supramesopleural sclerite [Ogata, 1991; Bouidinet, 2015]. sclerotised in Myrmica lobicornis (Figs 41–42), Pogon- The comparison between three female castes of Myrme- omyrmex badius (Figs 24, 49) or Aphaenogaster gibbosa cina nippomica Wheeler, W.M., 1906 (alate queen, in- (Figs 35–36), but are more heavily sclerotised in Manica termorphic queen and worker) undertaken by Miyazaki et rubida (Figs 43–44) and Messor denticulatus (Figs 47– al. [2005] revealed in particular that unlike the alate 48). A small distinctive micro-cone with an apical fora- queen, in which the spiracle is hidden between the me- men conceals the spiracle atrium at the cuticle of Atta sopleuron and metapleuron, the intermorphic queen has sexdens (Figs 45–46). In all dissected specimens of Myr- an invaginated cuticle around the spiracle opening, so the micinae workers the spiracular muscle could not be found. spiracle lies inside the hole located at the mesopleuron — The same problem concerns workers of Eciton burchellii metapleuron boundary that was not as conspicuous as in (Ecitoninae) that also have an exposed metathoracic alate queens; meanwhile the spiracle opening of the spiracle, but the spiracular entrance is located deeper worker is located at the inconspicuous boundary between than in Myrmicinae species (at the bottom of a short the two pleurons. As was revealed in the present study tubule) and is equipped with two markedly sclerotised regarding alate forms of other Myrmicinae species (Atta valves: the larger one somewhat resembles the opercu- sexdens, Manica rubida, Myrmica ruginodis), their sec- lum in its shape and position (Figs 33–34). ond spiracle really lies in a membranous area between the upper opposite edges of the meso- and metapleuron, and Discussion and conclusions its valves are scarcely sclerotised. Moreover, unlike the above mentioned subfamilies, the spiracular atrium of studied Myrmicinae workers (Aphaenogaster gibbosa, Despite the use of data on the state of metathoracic Manica rubida, Messor denticulatus, Myrmica lobicor- spiracles in modern taxonomic and phylogenetic studies nis, Pogonomyrmex badius) is provided with two valves, on Formicidae, the homology between the supramesopleu- similar in shape and size. These nearly membranous or ral sclerite of alate forms and the spiracular lobe of more strongly sclerotised valves can be observed exter- workers was not established until now. Meanwhile, the nally. Therefore, it seems natural that the absence of the Metathoracic spiracles in ants and wasps 61 protective sclerite in Myrmicinae females determined the as well as the photo editing were supported by the Russian exposed type of metathoracic spiracles in worker ants. Science Foundation project no. 15-29-02445. Nevertheless, in some cases the spiracle may be con- cealed. In particular, in Atta sexdens workers the cuticu- References lar micro-cone covers the true spiracle, thereby becoming a functional analogue of the vestibule chamber formed by Bohart R.M., Menke AS. 1976. Sphecid Wasps of the World: A Generic the supramesopleural sclerite in workers of the above Revision. Berkeley: University of California Press. 694 pp. Formicidae subfamilies. Boudinet B.E. 2015. Contributions to the knowledge of Formicidae In Dorylinae males, the true metathoracic spiracle (Hymenoptera, Aculeata): a new diagnosis of the family, the first instead of distinct sclerite is protected by two opposite global male-based key to subfamilies, and a treatment of early branching lineages // European Journal of . Vol.120. projections of the meso- and metapleural edges. The P.1–62. original description of the Dorylus labiatus spiracle Delye G. 1965. Anatomie et fonctionnement des stigmates de quelques supports that at least in males, it is provided with a fan- fourmis (Hyménoptères Formicidae) // Insectes Sociaux. Vol.12. shaped occlusor muscle attached to the differentiated P.285–290. Deyrup M., Cover S. 2004. A new species of Odontomachus ant operculum, and the muscle “takes its origin on an inter- (Hymenoptera: Formicidae) from inland ridges of Florida, with nal arched sclerotised ridge of the postero-dorsal corner a key to the Odontomachus of the United States // Florida of the mesepimeron” [Tonapi, 1959:88]. The state of Entomologist. Vol.87. P.136–144. http://dx.doi.org/10.1653/ the second spiracles in workers of the examined Doryli- 0015-4040(2004)087[0136:ANSOOA]2.0.CO;2. nae and Ecitoninae species are characterised now as Duncan C.D. 1939. A contribution to the biology of North American vespine wasps // Stanford University Publications Biological exposed because the spiracular lobe is absent [Keller, Sciences. Vol.8. P.1–272. 2011], but their internal structure needs additional study. Emery C. 1900. Intorno al torace delle formiche e particolarmente dei Unfortunately, the methods applied in the current neutri // Bullettino della Societa‘ Entomologica Italiana. Vol.32. study were insufficient to determine the presence or P.103–119. Keller R.A. 2011. A phylogenetic analysis of ant morphology (Hy- absence of muscles in exposed metathoracic spiracles of menoptera: Formicidae) with special reference to the poneromor- Myrmicinae and Ecitoninae ant workers. However, even ph subfamilies // Bulletin of the American Museum of Natural the external comparison revealed some inequalities in History. Vol.355. P.1–90. http://dx.doi.org/10.1206/355.1. spiracle structure between both subfamilies. In particular MacGown J.A., Boudinot B.E., Deyrup M., Sorger D.M. 2014. A the atrium of the second spiracle in Eciton burchellii, in review of the Nearctic Odontomachus (Hymenoptera: Formi- cidae: Ponerinae) with a treatment of the males // Zootaxa. contrast to Myrmicinae species, lies in a short tubule and Vol.3802. P.515–552. http://dx.doi.org/10.11646/zoot- the spiracular valves are markedly different. axa.3802.4.6. The authors of a comprehensive morphological in- Miyazaki S., Murakami T., Azuma N., Higashi S., Miura T. 2005. vestigation în the musculature and skeleton of Hy- Morphological differences among three female castes: worker, queen and intermorphic queen in the ant Myrmecina nipponica menoptera [Vilhelmsen et al., 2010] suggested that the (Formicidae: Myrmicinae) // . Vol.46. P.363–374. presence of the supramesopleural sclerite is one of puta- Nasonov N.V. 1889. [Contribution to the natural history of tive autapomorphies of Aculeata. The results of the present primarily of Russia (Formicariae, Formicidae): Part 2. Contribu- study indicated that in addition to sclerite, which conceals tions to the anatomy of the ant (Lasius flavus Fabr)] // Izvestiya the metathoracic spiracle, the representatives of Vespi- Imperatorskago Obshchestva Lyubitelei Estestvoznaniya, Antropologii i Etnografii. Vol.58. P.1–42 + I–IX [in Russian]. dae as well as species of several Formicidae subfamilies Ogata K. 1987. A generic synopsis of the poneroid complex of the have a spiracular mechanism similar to their mesothorac- family Formicidae in Japan (Hymenoptera). Part I. Subfamilies ic spiracle. It is quite probable that the muscle essential to Ponerinae and Cerapachyinae // Esakia. Vol.25. P.97–132. the second thoracic spiracle of Symphyta [Vilhelmsen, Ogata K. 1991. A generic synopsis of the poneroid complex of the family Formicidae (Hymenoptera) in Japan. Part II. Subfamily 2000; Vilhelmsen et al., 2010] and the re-discovered Myrmicinae // Bulletin of the Institute of Tropical Agriculture, spiracular muscle in Aculeata are homologous. Kyushu University. Vol.14. P.61–149. Reid J.A. 1941. The thorax of wingless and shortwinged Hymenoptera ACKNOWLEDGEMENTS. This work continues the com- // Transactions of the Royal Entomological Society of London. parative anatomical research on ants initiated by Professor Vol.91. P.361–446. Richards O.W. 1977. Hymenoptera. Introduction and key to families Gennady Dlussky. However numerous other colleagues con- nd tributed as well. Dr. Anatoly Zakharov from A.N. Severtsov (2 ed.). Handbooks for the identification of British 6(1). London: Royal Entomological Society of London. 100 pp. Institute of Ecology and provided various ant spec- Snodgrass R. E. 1925. Anatomy and physiology of the honeybee. imens as well as a place for dissection equipped with a stereom- New York: McGraw-Hill. 327 pp. icroscope and other needed materials. All of the scanning Tonapi G.T. 1958. A comparative study of spiracular structure and electron microscopy work was done at IPEE RAS, and I thank mechanisms in some Hymenoptera // Transactions of the Royal Nadezhda Surovenkova. The team at the Laboratory of Arthro- Entomological Society of London. Vol.110. P.489–532. pods and especially Professor Alexander Rasnitsyn and Dmit- Tonapi G.T. 1959. A note on the respiratory system of the male of ry Shcherbakov from A.A. Borissiak Palaeontological Insti- Dorylus labiatus Shuck. // Proceedings of the Indian Academy tute RAS consulted with me on working with Leica and its of Sciences, Section B. Vol.49. P.87–93. digital camera. Both preparation and dissection of needed Vilhelmsen L. 2000. Before the wasp-waist: comparative anatomy and phylogenetic implications of the skeleto-musculature of the samples were carried out with financial support by the Re- thoraco-abdominal boundary region in basal Hymenoptera (In- search project of MSU Zoological Museum (AAAA-A16- secta) // Zoomorphology. Vol.119. P.185–22. http://dx.doi.org/ 116021660077-3). The scanning electron microscopy of se- 10.1007/PL00008493. lected specimens was funded by the Russian Science Founda- Vilhelmsen L., Mikó I., Krogmann L. 2010. Beyond the wasp-waist: tion project no. 12-04-01071. The photographing of wet mounts structural diversity and phylogenetic significance of the meso- 62 E.B. Fedoseeva

soma in apocritan wasps (Insecta: Hymenoptera) // Zoological 5 (12): e15991. http://dx.doi.org/10.1371/journal.pone.0015991 Journal of the Linnean Society. Vol.159. P.22–194. http:// Yoshimura M., Fisher B.L. 2012. A revision of male ants of the dx.doi.org/10.1111/j.1096-3642.2009.00576.x. Malagasy (Hymenoptera: Formicidae) with res- Yoder M.J., Mikó I., Seltmann K.C., Bertone M.A., Deans A.R. urrections of the genera Stigmatomma and Xymmer // PLoS ONE 2010. A gross anatomy ontology for Hymenoptera // PLoS ONE 7: e3325.http://dx.doi.org/10.1371/journal.pone.0033325.

APPENDIX 1 Material examined

Abbreviations in the Appendix : * f — female, m — male, w — worker. ** Canberra — Australia, Canberra; Cam-Ranh — Vietnam, Cam-Ranh; Lake Louise — Canada, Alta: Lake Louise, 150 km W of Calgary; Moscow — Russia, Moscow; Muhtumkuli — Turkmenistan, Balkan Dep., Muchtumkuli (Kara-Kala); Nam Cat Tien — Vietnam, Dong Nai Prov., Nam Cat Tien;Narofominsk — Russia, Moscow Region, Narofominsk District; Peshki — Russia, Moscow Region, 55 km N-W Moscow; Pinezhsky NR — Russia, Arkhangelsk Region, Pinezhsky District, Pinezhsky Nature Reserve; Pukalpa — Peru, Dep. Ukayali, 60 km W Pukalpa; Sonoyta — Mexico, State Sonora, Sonoyta; Teberda — Russia, Karachaevo-Cherkesia Rep., Teberdinsky Zapovednik. *** SEM — scanning electron microscopy; DC — digital camera. APPENDIX 2 List of abbreviations used in Figures 1–9 arm2 — operculum arm of the metathoracic spiracle ular lobe at2 — atrium of the metathoracic spiracle pr — propodeum lw — projection of the anterior metapleural edge psp — propodeal spiracle mi — micro-cone above the metathoracic spiracle r2 — immovable rim of the metathoracic spiracle mn — mesonotum rug — cuticular rugae around the metathoracic spiracle msmts — mesometapleural suture sms — supramesopleural sclerite mspl — mesopleuron sp1 — mesothoracic spiracle mtpc — metapleural carina sp2 — metathoracic spiracle mtpl — metapleuron spl — spiracular lobe occ1 — occlusor muscle of the mesothoracic spiracle tr1 — trachea of the mesothoracic spiracle occ2 — occlusor muscle of the metathoracic spiracle tr2 — trachea of the metathoracic spiracle op2 — operculum of the metathoracic spiracle up — projection of the posterior mesopleuron edge or — orifice in the supramesopleural sclerite and spirac- vv — spiracular valves